animals Article Forgotten, But Not Lost—Alloparental Behavior and Pup–Adult Interactions in Companion Dogs Péter Pongrácz * and Sára S. Sztruhala Department of Ethology, Eötvös Loránd University, Pázmány Péter sétány 1/c, 1117 Budapest, Hungary; [email protected] * Correspondence: [email protected] Received: 30 October 2019; Accepted: 14 November 2019; Published: 21 November 2019 Simple Summary: Companion dogs are vastly popular animals; however, we know surprisingly little about their natural parental behaviors. Meanwhile, although wolves, dingoes, and, to an extent, even free-ranging dogs show several forms of alloparental behaviors, the parental care among companion dogs is thought to be solely provided by the mother. We circulated an international survey for dog breeders, asking them about the forms of alloparental behaviors they observed among their dogs, as well as further interactions between the puppies and other adult dogs at home. Our results show that allonursing and feeding of the pups by regurgitation is a widespread phenomenon among companion dogs. The behavior of young puppies regarding, for example, their reaction to other dogs’ barking was also influenced by the timing of their access to the other dogs at the breeder’s home. Based on the breeders’ observations, sexual status and age of the other dogs affected the way they interacted with the puppies, and also the way the puppies’ mother interacted with them. These results highlight the importance of dog–puppy interactions during the early weeks of life, an often neglected area compared to the well-known elements of puppy socialization with human beings. Abstract: Socialization with humans is known to be a pivotal factor in the development of appropriate adult dog behavior, but the role and extent of dog–dog interactions in the first two months of life is rarely studied. Although various forms of alloparental behaviors are described in the case of wild-living canids, the social network of companion dogs around home-raised puppies is almost unknown. An international online survey of companion dog breeders was conducted, asking about the interactions of other dogs in the household with the puppies and the pups’ mother. Based on the observations of these breeders, our study showed an intricate network of interactions among adult dogs and puppies below the age of weaning. Alloparental behaviors (including suckling and feeding by regurgitation) were reportedly common. Independent of their sex, other household dogs mostly behaved in an amicable way with the puppies, and in the case of unseparated housing, the puppies reacted with lower fear to the barks of the others. Parousness, sexual status, and age of the adult dogs had an association with how interested the dogs were in interacting with the puppies, and also with how the mother reacted to the other dogs. Our study highlights the possible importance of dog–dog interactions during the early life of puppies in forming stable and low-stress interactions with other dogs later in life. Keywords: behavior; dog; alloparental care; puppies; breeders 1. Introduction The species-specific traits of dogs (Canis familiaris) are mostly inseparable from the process of domestication. The evolutionary changes in the socio-cognitive capacities [1,2], behavior [3,4], anatomy and physical appearance [5,6], as well as the physiology [7,8], are most often evaluated Animals 2019, 9, 1011; doi:10.3390/ani9121011 www.mdpi.com/journal/animals Animals 2019, 9, 1011 2 of 17 with regard to the differences between dogs and their closer or more distant wild-living relatives. More recently, researchers concentrated on the behavioral and cognitive features [9,10], both as proximate and ultimate factors behind the adaptation of dogs to the anthropogenic niche, with only a few exceptions—for example, genetic changes that could affect the carbohydrate metabolism in dogs were also highlighted as assumed key factors behind domestication [11,12]. Although differences in the reproductive biology of dogs (e.g., switching from being monestrous to a mainly diestrous cycle), when compared to their closest wild relative, the grey wolf (Canis lupus), are also apparent among the crucial changes, and have also been modeled by the well-known silver fox project conducted in Novosibirsk, Russia [13], the reproductive behavior of companion (or “family”) dogs is rarely discussed in scientific literature, apart from various issues covered by veterinary science (e.g., [14,15]). As the reproduction of companion (and working) dogs is mainly planned, supervised, and restricted by human caretakers [16,17], this segment of dog behavior remains almost untouched by ethologists. Furthermore, alloparental behavior and paternal caretaking of the young, two factors which are considered uniquely typical for a wide selection of canid species [18], are literally unknown among companion dogs, and have only recently been discovered in the free-ranging dog populations [19,20]. Free-ranging dogs are often considered to be the “ecologically most successful” variants of domestic dogs due to their vast number (according to some estimations, around 800 million worldwide—[21]) and ubiquitous presence in and around human settlements. Subsequently, it is assumed that free-ranging dogs provide the best opportunity to understand the biology of dogs [21], as free-ranging dogs have been adapting to their environment for many generations without excessive artificial selection by humans. However, when it comes to parental behavior, seemingly, there is a considerable difference, even among free-ranging dogs. This has led to such widely differing observations, which have either stated that lack of alloparental care is one of the reasons why mortality rate of young pups is very high among free-ranging dogs (in Italy—[22]; in Mexico—[23]), or described more or less sporadic, but existing paternal/alloparental caretaking (in India—[20,24]). In their exhaustive review on canid reproduction, Lord and colleagues [25] assumed that since domestic dogs became dependent on human resources, they mostly lost the need for alloparental caretaking (i.e., because they have a stable food supply); meanwhile, the same ecologically predictable food resources made it possible that the sexual behavior of dogs also mostly lost the strict seasonality that is typical to wild canids. This feeding ecology-based theory gains further (indirect) support from the observations made with dingoes—feral dogs in Australia that became isolated from other Southeastern Asian dog populations around 3.5–5 thousand years ago [26]. These dogs sustain themselves mainly by hunting large prey—consequently, they have retained many typical features of the reproductive behavior of wolves (e.g., alloparental care—[27], monestrus—[18]), because these seem to support the lifestyle of apex canid predators. Very little is known about the natural interactions of juvenile (pre- and around weaning period) dogs and their older canine companions (kin and non-kin) in the case of companion (pet) and working dogs. Contrary to dog–human interactions during puppyhood, which were recently investigated from multiple aspects and considered to be a crucial part of the “process of proper socialization” [3,28–30], the behavior and effect of adult dogs on puppies in the home environment have received much less interest from investigators. Among the most likely reasons for this is the difficulty of conducting observations at the owners’ home, or the highly variable social environment (i.e., there is no standardized or “natural” social structure at breeders’ homes that would include roughly the same kinds of adult dogs around the puppies). Consequently, although there are data about the interactions of dog puppies with other dogs at public areas [31], as well as pup–pup interactions within the litter (e.g., the ontogeny of playful behavior [32]), our knowledge of pups’ interactions with familiar, but not necessarily related adult dogs from the household is very limited. The exception is the interaction with the mother—as the extent and style of maternal care was found to have fundamental effects on later behavior in working dogs (e.g., drug seeking dogs—[33]; police dogs—[34]). However, except for the work of [35] regarding the feeding of the pups by regurgitation, we do not know of any studies on alloparental behavior within pet dog groups, and indications of paternal care are missing as well. Animals 2019, 9, 1011 3 of 17 In this study, we conducted a detailed, international internet questionnaire about alloparental behavior and pup–adult dog interactions within companion dog groups that live at the homes of dog breeders. We surveyed not only the existence of alloparental nursing and feeding of pups by regurgitation, but we also covered such behaviors as the mother dog’s reaction to other adult dogs around her offspring, and the pups’ reaction to other household dogs’ barking. We analyzed whether the aforementioned behavioral variables were dependent on the circumstances of how the pups were kept—especially with regard to their isolation from the other dogs in the home. Based on the literature about the reproductive biology of free-ranging dogs [36] and dingoes (e.g., [18]) (both of which are not under direct human control), it can be assumed that alloparental behavior emerges in dogs as a functional response of the temporal predictability and ease of access to food [25]. As companion and working dogs in private or professional kennels are steadily provided with easily accessible food, one could assume that the need for alloparental and paternal care is minimal to non-existent. However, as an alternative hypothesis, one could expect that even companion dog populations have retained the capacity of providing alloparental care, as we do not know about active selection that would go against this capacity in dogs under human management. 2. Materials and Methods 2.1. Ethical Approval This study was carried out in accordance with national and international ethical guidelines (e.g., American Psychological Association, Hungarian Psychological Association).